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The Sampling Scheme Matters: Pan Troglodytes Troglodytes and P

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The Sampling Scheme Matters: Pan Troglodytes Troglodytes and P AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 156:181–191 (2015) The Sampling Scheme Matters: Pan troglodytes troglodytes and P. t. schweinfurthii Are Characterized by Clinal Genetic Variation Rather Than a Strong Subspecies Break Tillmann Funfst€ uck,€ 1* Mimi Arandjelovic,1 David B. Morgan,2 Crickette Sanz,3 Patricia Reed,2 Sarah H. Olson,2 Ken Cameron,2 Alain Ondzie,4 Martine Peeters,5 and Linda Vigilant1* 1Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany 2Wildlife Conservation Society, Global Conservation, 2300 Southern Boulevard, New York, NY 10460, USA 3Department of Anthropology, Washington University, 1 Brookings Drive, Saint Louis, MO 63130, USA 4Wildlife Conservation Society, Congo Program, 151 Ave Charles de Gaulle, Brazzaville, Republic of Congo 5UMI233, TransVIHMI, Institut de Recherche pour le Developpement (IRD) and Universite Montpellier 1, Montpel- lier, France KEY WORDS genetic differentiation; isolation by distance; structure; microsatellites; genotyping ABSTRACT Populations of an organism living in were sampled across large parts of their range and analyzed marked geographical or evolutionary isolation from other them together with 283 published eastern chimpanzee geno- populations of the same species are often termed subspecies types from known localities. We observed a clear signal of and expected to show some degree of genetic distinctiveness. isolation by distance across both subspecies. Further, we Thecommonchimpanzee(Pan troglodytes) is currently found that a large proportionofcomparisonsbetween described as four geographically delimited subspecies: the groups taken from the same subspecies showed higher western (P. t. verus), the nigerian-cameroonian (P. t. ellioti), genetic differentiation than the least differentiated the central (P. t. troglodytes) and the eastern (P. t. schwein- between-subspecies comparison. This proportion decreased furthii) chimpanzees. Although these taxa would be substantially when we simulated a more clumped sampling expected to be reciprocally monophyletic, studies have not scheme by including fewer groups. Our results support the always consistently resolved the central and eastern chim- general concept that the distribution of the sampled individ- panzee taxa. Most studies, however, used data from individ- uals can dramatically affect the inference of genetic popula- uals of unknown or approximate geographic provenance. tion structure. With regard to chimpanzees, our results Thus, genetic data from samples of known origin may shed emphasize the close relationship of equatorial chimpanzees light on the evolutionary relationship of these subspecies. from central and eastern equatorial Africa and the difficult We generated microsatellite genotypes from noninvasively nature of subspecies definitions. Am J Phys Anthropol collected fecal samples of 185 central chimpanzees that 156:181–191, 2015. VC 2014 Wiley Periodicals, Inc. INTRODUCTION Additional Supporting Information may be found in the online Understanding the distribution of genetic variation version of this article. within an endangered species such as the common chim- panzee, Pan troglodytes, is crucial for elucidating its evo- Abbreviations: HWE, Hardy-Weinberg equilibrium; IBD, isolation lutionary history (Morin et al., 1994; Stone et al., 2002; by distance; LD, linkage disequilibrium; MCP, minimum convex Gonder et al., 2006; Becquet et al., 2007), especially polygon; because there is an almost complete absence of a fossil Grant sponsor: Max Planck Society, the Arcus Foundation, the record (McBrearty and Jablonski, 2005). In addition, Paul G. Allen Family Foundation, the Dunemere Foundation, the knowledge of population relationships might also facili- Bradley L. Goldberg Foundation, the Societ e pour la Conservation tate the use of the limited resources available for conser- et le Developpement (SCD), the Wildlife Conservation Society vation efforts (Schonewald-Cox et al., 1983; Avise, 1996) (WCS).; Grant sponsor: National Institutes of Health; Grant num- and help in guiding breeding programs of chimpanzees ber: R01 AI50529.; Grant sponsor: Agence Nationale de Recherches kept in captivity (reviewed in Witzenberger and Hoch- sur le SIDA, France; Grant number: ANRS 12255. kirch, 2011; Hvilsom et al., 2013). Arguing on the basis of morphological or genetic evi- *Correspondence to: Tillmann Funfst€ uck;€ Max Planck Institute for Evolutionary Anthropology; Deutscher Platz 6; 04103 Leipzig; dence and consideration of geographic distribution, Germany. E-mail: [email protected] or Linda Vigi- researchers have separated Pan troglodytes into three lant; E-mail: [email protected] different subspecies: the western chimpanzee (P. t. verus), the central chimpanzee (P. t. troglodytes), and the Received 12 May 2014; accepted 6 October 2014 eastern chimpanzee (P. t. schweinfurthii) (e.g. Hill, 1969; Morin et al., 1994; Groves, 2001; Becquet et al., 2007). DOI: 10.1002/ajpa.22638 Later, the existence of a fourth subspecies, the Nigerian- Published online 20 October 2014 in Wiley Online Library Cameroonian chimpanzee, P. t. ellioti (Oates et al., (wileyonlinelibrary.com). Ó 2014 WILEY PERIODICALS, INC. 182 T. FUNFST€ UCK€ ET AL. Fig. 1. The map of Africa on the left side indicates the ranges of chimpanzee subspecies (yellow: P. t. verus, green: P. t. ellioti, red: P. t. troglodytes, blue: P. t. schweinfurthii). The zoomed in maps on the right illustrate the region sampled for the present study with blue and red dots depicting sampling locations. The red dots refer to geographically outlying samples that were not assigned to a certain group for calculations of IBD and genetic differentiation (see Methods). National borders are in red, national parks in yellow, rivers in blue and roads in white. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary. com.] 2009), originally termed P. t. vellerosus, was suggested which individuals found closer together are genetically (Gonder et al., 1997). The validity of that taxon was sup- more similar than those further apart, and it arises ported by studies utilizing mitochondrial DNA (mtDNA) when the distance an individual may disperse is smaller (Gonder et al., 1997; Gagneux et al., 1999; Gonder et al., than the continuous distribution of the organism 2006; Bjork et al., 2010), microsatellite loci (Gonder (Wright, 1943). To detect such a cline in genetic varia- et al., 2011), autosomal sequence data (Bowden et al., tion one needs to use samples of known geographic ori- 2012) as well as complete genomes (Prado-Martinez gin sampled according to a pattern that is as little et al., 2013). Thus, the currently most widely accepted clumped and as widespread as possible. However, most taxonomy of the common chimpanzee splits them into studies that detected clearly separated subspecies of Pan four geographically defined subspecies (Fig. 1), separated troglodytes used, at least partly, samples with unknown from each other from west to east by the Dahomey gap, exact origins or rather clustered sampling schemes (Bec- the Sanaga River and the Ubangi River. quet et al., 2007; Bowden et al., 2012; Prado-Martinez However, this classification is not without controversy. et al., 2013). Fischer et al. (2006) generally questioned the subspecies Although not challenging the concept of chimpanzee concept in Pan troglodytes. Using nuclear nonrepetitive subspecies in general, some authors have suggested that DNA sequences they found an extent of genetic differen- central and eastern chimpanzees do not represent geo- tiation among subspecies comparable to that seen among graphically separated subspecies, but might rather form human populations. They speculated that a more one taxon of equatorial chimpanzees. Specifically, mor- geographically-informed sampling would reveal a pat- phological studies found a close dental (Pilbrow, 2006) tern of isolation by distance (IBD) as has been described and cranial (Guy et al., 2003) similarity between P. t. for within-continental variation in humans (Serre and troglodytes and P. t. schweinfurthii. Studies describing Pa€abo,€ 2004; Rosenberg et al., 2005; Lao et al., 2008; the distribution of genetic variation within chimpanzees Tishkoff et al., 2009). IBD describes the situation in could potentially evaluate the evolutionary independence American Journal of Physical Anthropology STRUCTURE OF EQUATORIAL CHIMPANZEES 183 of these taxa by investigating if monophyletic clades of For the present study noninvasively collected fecal central and eastern chimpanzees are found. Gagneux samples of 185 central and published genotypes from et al. (1999), analyzing mtDNA sequences of 154 eastern 283 eastern chimpanzees of known geographic origin and 24 central chimpanzees, found the eastern clade to were used. The origins of the individuals were as contin- be nested within the central clade, thereby raising the uously distributed as was feasible and included central question if these two subspecies should not be regarded and eastern chimpanzees from their western- and as one clade of equatorial chimpanzees. Later studies eastern-most range, respectively. We generated geno- including more mtDNA haplotypes again did not find types at 12 microsatellite loci and analyzed them by consistent support for monophyly of P. t. troglodytes and applying multiple methods. We used a Bayesian based P. t. schweinfurthii (Gagneux et al., 2001; Gonder et al., clustering algorithm implemented in STRUCTURE as 2006). In addition,
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